Physiological Mechanisms Constraining Ectotherm Fright-Dive Performance at Elevated Temperatures Essie M

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Physiological Mechanisms Constraining Ectotherm Fright-Dive Performance at Elevated Temperatures Essie M © 2017. Published by The Company of Biologists Ltd | Journal of Experimental Biology (2017) 220, 3556-3564 doi:10.1242/jeb.155440 RESEARCH ARTICLE Physiological mechanisms constraining ectotherm fright-dive performance at elevated temperatures Essie M. Rodgers and Craig E. Franklin* ABSTRACT such as locomotor performance (Johansen and Jones, 2011), Survival of air-breathing, diving ectotherms is dependent on their developmental rates/growth (McLeod et al., 2013), immune capacity to optimise the time available for obligate underwater competence (Yu et al., 2009) and survival (Rohr and Palmer, 2013). activities, such as predator avoidance. Submergence times are The consequences of elevated temperatures on ectotherm thermally sensitive, with dive durations significantly reduced by performance are well documented (Bellard et al., 2012; increases in water temperature, deeming these animals particularly Kingsolver et al., 2013) but the physiological basis for loss of vulnerable to the effects of climate change. The physiological performance remains unclear. Performance decrements at mechanisms underlying this compromised performance are unclear stressfully high temperatures are hypothesised to stem from but are hypothesised to be linked to increased oxygen demand and a oxygen demand exceeding oxygen supply capacity [i.e. cardio- reduced capacity for metabolic depression at elevated temperatures. respiratory system failure; oxygen- and capacity-limited thermal Here, we investigated how water temperature (both acute and chronic tolerance (OCLTT) hypothesis] (Pörtner, 2001, 2010; Pörtner and exposures) affected the physiology of juvenile estuarine crocodiles Knust, 2007; Pörtner and Farrell, 2008; Eliason et al., 2011). Compromised aerobic performance may occur at high temperatures (Crocodylus porosus) performing predator avoidance dives (i.e. ̇ ‘ ’ when maximal rates of oxygen consumption (VO ,max) plateau or fright-dives). Diving oxygen consumption, fright bradycardia, ̇ 2 haematocrit and haemoglobin (indicators of blood oxygen carrying decrease but resting/standard metabolic rate (VO2,standard) increases ̇ − ̇ capacity) were assessed at two test temperatures, reflective of exponentially, reducing absolute aerobic scope (=VO2,max VO2,standard). different climate change scenarios (i.e. current summer water A narrowed aerobic scope is thought to translate into a reduced temperatures, 28°C, and ‘high’ climate warming, 34°C). Diving capacity for activities including growth, movement, digestion and oxygen consumption rate increased threefold between 28 and 34°C reproduction (Pörtner, 2002), and the thermal effects on individuals may scale up to affect population and community dynamics (Pörtner (Q10=7.4). The capacity to depress oxygen demand was reduced at elevated temperatures, with animals lowering oxygen demand from and Peck, 2010). A narrowed aerobic scope at high temperatures has surface levels by 52.9±27.8% and 27.8±16.5% (means±s.e.m.) been demonstrated in a number of tropical ectotherms (Munday at 28°C and 34°C, respectively. Resting and post-fright-dive et al., 2009; Nilsson et al., 2009; Johansen and Jones, 2011; haematocrit and haemoglobin were thermally insensitive. Together Rummer et al., 2014); however, the OCLTT hypothesis is not these findings suggest decrements in fright-dive performance at universal (Clark et al., 2013; Ern et al., 2014, 2015, 2016; Norin elevated temperatures stem from increased oxygen demand coupled et al., 2014). Many ectotherms experience compromised with a reduced capacity for metabolic depression. performance at temperatures below those affecting aerobic scope (Norin et al., 2014), suggesting the mechanistic explanation may be KEY WORDS: Aerobic dive limit, Diving metabolism, Thermal multi-faceted and thus it remains unresolved in many taxa. sensitivity, Climate change, Bradycardia, Heart rate Air-breathing, diving ectotherms (e.g. sea snakes, marine iguanas, turtles and crocodylians) appear vulnerable to increases INTRODUCTION in water temperature as dive capacity (i.e. time spent submerged/ The performance and survival of many ectothermic species is dive duration) is inversely related to water temperature (Fuster et al., predicted to be compromised under global climate change (Pörtner 1997; Prassack et al., 2001; Priest and Franklin, 2002). Shortened and Farrell, 2008). Altered thermal regimes are particularly dive times translate into less time available for obligate underwater threatening to ectotherms (almost all fish, amphibians and activities such as foraging/hunting, predator avoidance, sleep/rest reptiles) as body temperature is closely tied to the thermal and social interactions. Submergence times of free-ranging environment. Ectotherm performance is optimised within a crocodylians and turtles are reduced in summer months compared limited range of body temperatures (i.e. thermal performance with winter months (Carr et al., 1980; Bentivegna et al., 2003; breadth) and ongoing climate warming will probably drive Gordos et al., 2003; Hochscheid et al., 2005; Bradshaw et al., 2007; temperatures beyond sustainable limits (Rummer et al., 2014). Campbell et al., 2010a), suggesting these animals are not fully Body temperatures surpassing thermal performance optima are compensating for present-day seasonal thermal fluctuations. Dive generally accompanied by a marked decline in fitness-related traits durations are predicted to be further reduced by ongoing increases in water temperature in marine and freshwater habitats, with submergence times of some species forecasted to halve under a School of Biological Sciences, The University of Queensland, St Lucia, Brisbane, QLD 4072, Australia. moderate rate of climate warming (SRES A1B storyline; 50th percentile of IPCC global warming range; Rodgers et al., 2015). A *Author for correspondence ([email protected]) limited or non-existent capacity to thermally acclimate/acclimatise C.E.F., 0000-0003-1315-3797 to elevated temperatures following long-term (i.e. chronic) exposure elevates the susceptibility of this group to climate Received 22 December 2016; Accepted 25 July 2017 change (Clark et al., 2008; Rodgers et al., 2015), but physiological Journal of Experimental Biology 3556 RESEARCH ARTICLE Journal of Experimental Biology (2017) 220, 3556-3564 doi:10.1242/jeb.155440 animal escapes/dives underwater in response to a perceived threat List of abbreviations (e.g. loud noise or the presence of an experimenter; Wright et al., ADL aerobic dive limit 1992). Diving is a vital pre-condition for the onset of fright fH heart rate bradycardia and heart rate does not drop in C. porosus in response to OCLTT oxygen- and capacity-limited thermal tolerance a threat on land (Wright et al., 1992). The mechanism underlying the RQ respiratory quotient thermal sensitivity of fright-dive performance probably differs TBO total body oxygen ̇ from OCLTT, which does not consider hypometabolic states. High VO oxygen consumption rate ̇ 2 VO ,dive diving oxygen consumption rate temperatures may not only elevate fright-dive metabolic rate ̇ 2 ̇ ’ VO2,post-dive post-fright-dive oxygen consumption rate (VO ,dive) but also compromise a diver s capacity to depress ̇ 2 VO2,pre-dive surface/pre-fright-dive oxygen consumption rate metabolic rate from resting/surface levels. V̇ standard oxygen consumption rate O2,standard The aim of this study was to investigate how the fright-dive physiology of juvenile estuarine crocodiles is affected by increases in water temperature. Crocodylians are primarily aquatic, and free- mechanisms constraining performance at high temperatures ranging animals have been recorded to dive 50–70 times per day remain uncertain. (Campbell et al., 2010a). The ability to remain submerged for The aerobic dive limit (ADL) conceptually represents the extended periods of time is thought to be adaptive because predator maximum duration an animal can remain submerged before avoidance, foraging, sleep/recovery and social interactions occur oxygen debt is incurred (Butler, 2006). An individual’sADLis underwater (Seebacher et al., 2005; Campbell et al., 2010b). dependent on total body oxygen (TBO) stores and the rate at which Predator escape dives are vital in hatchling and juvenile C. porosus, these stores are consumed, with smaller stores and/or a faster rate of which may fall prey to a range of species including: monitor lizards oxygen consumption reflective of a shorter ADL (Butler, 2006). (Varanus mertensi, Varanus panoptes), barramundi (Lates Oxygen can be stored in the lungs, blood and tissue, and the calcarifer), whistling kites (Haliastur sphenurus), olive pythons percentage contribution of stores varies between species (Kooyman, (Liasis olivasceus), great egrets (Ardea alba) and larger C. porosus 1989). In estuarine crocodiles (Crocodylus porosus), for instance, (Grigg and Kirshner, 2015). The fright-dive capacity of juvenile pulmonary (i.e. lung) oxygen represents the majority of stores C. porosus is thermally sensitive, with marked reductions in dive (∼67.0%), followed by blood oxygen (∼28.9%), and tissue oxygen duration at temperatures above 28°C (Rodgers et al., 2015), but the contributes the least (∼4.1%) (Wright, 1985). Ectotherm oxygen physiological mechanism underlying this pattern is unresolved. We stores decline with increasing temperature (Pough, 1976; Fuster et al., assessed the effect of water temperature on V̇ and fright ̇ O2,dive 1997); however, dive duration is reduced at elevated temperatures bradycardia. We hypothesised that VO2,dive would increase
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